1. Introduction
Microscopic fungi represent an important component in the peat soils of the polar ecosystems in the Arctic and Subarctic regions. They are a link in the biogeochemical processes of peat formation [1,2], despite a simplified trophic structure [3,4,5] and a shortened life cycle in soils of Subarctic and Arctic terrestrial ecosystems [6]. Microscopic fungi actively produce various organic acids during the metabolism process [7]. This promotes the transformation of hard-to-decompose plant litter [4,5,8,9,10]. The abundance and diversity of soil microscopic fungi is better determined by the effect of abiotic factors: temperature, large temperature fluctuations, high UV radiation, osmotic pressure, etc. [11,12], as well as anthropogenic impacts [13]. To maintain stability and stabilization under permafrost conditions [12,14,15,16], fungi use various adaptation mechanisms [17,18,19,20,21,22,23,24]. Studies on the biodiversity of soil microorganisms in the Arctic and Antarctic systems have been conducted for a long time, and at present they cover various regions worldwide [25,26,27]. Microscopic fungi and their adaptive functions are actively studied in the soils of the McMurdo Dry Valleys of Antarctica [19,20,28,29], in the oligotrophic soils of continental Antarctica [30], in the active layers, permafrost and cryopegs of the Arctic [25,26,31], in the Arctic tundra of Spitsbergen [32,33] and in organic and mineral soils in the Alaskan Arctic [34]. Furthermore, in the investigation of microscopic fungi, special attention is focused towards studying their morphology, ecophysiology [35,36], ecology [37,38,39], molecular biology [40] and enzymology [41,42,43]. In permafrost-affected peat soils, researches are mainly aimed at (i) studying the community of bacteria and their association with the quality of organic material of peat [44], (ii) revealing the regularities of successional changes in microscopic fungal composition during sphagnum moss decomposition in the boreal peat soils of Canada within experimentations concerning climate change prediction [45,46], and (iii) studying the structure of soil microbial communities during natural regeneration of degraded peatlands in Scotland [47,48].
There were a few studies on the raised and lowland peatlands of the East European Plain and Western Siberia in Russia [49]. The specifics of composition and structure of soil microbial communities have been studied in permafrost-free peat soils [50], melted bogs of the boreal zone [49,51], active and permafrost layers of peat plateaus [3,4,5,52,53,54] and polygonal bogs and wetlands [55,56] of the Subarctic and Arctic areas of the European Northeast.
In view of insufficient study of the microscopic fungal composition and structure in the soils of the cryolitozone [4,5,31,54], and the lack of data on the distribution regularities of eukaryotes in the “Active layer-Permafrost layer” system, special attention should be paid to (i) studies of the microscopic fungal structure and functioning in the soils of permafrost-affected peat plateaus of the Arctic and Subarctic regions of the European Northeast of Russia, and (ii) identification of zonal and subzonal patterns in changes in their main parameters associated with the circulation of soil organic matter and the biogeochemical cycle [57].
Consequently, this study aims to investigate the species diversity and structure of microscopic fungi in permafrost peatlands of flatland areas in the cryolitozone of the European Northeast of Russia. Our main task is to compile a list of culturable microscopic fungi isolated and identified from peat deposits within peat plateaus of the forest-tundra and tundra. We hypothesized that the deterioration of climatic conditions in the direction from the forest tundra to the northern tundra should be reflected in a change in the qualitative and quantitative composition of fungal communities.
2. Study Area and Methods
2.1. Description of the Study Area
The study objects were the microfungal communities of peat soils of peat plateaus in the flatland areas of the European Northeast of Russia (Figure 1a). Peat plateaus (peatlands) are represented by permafrost-affected flat-topped mound bogs (frozen bogs). During this study, objects were selected to the extent that they belonged to different bioclimatic zones/subzones: forest-tundra zone (Plot 1 and 2), southern shrub tundra subzone (Plot 3 and 4) and typical northern tundra subzone (Plot 5 and 6) (Figure 1b, Table 1). In all plots, sampling was carried out within flat-topped peat mounds with well-defined vegetation cover composed of shrub-moss communities including Ledum decumbens, Betula nana, Rubus chamaemorus, mosses (Sphagnum fuscum, S. russowii, Polytrichum spp., Dicranum spp.) and lichens occurring mainly in hollows. The studied peatlands of peat mounds are represented by typical oligotrophic permafrost peatlands (Figure 2). The total thickness of peat deposits on each plot is about 240–270 cm. The exceptions are (i) Plot 2, where sampling was limited to a depth of 115 cm, and (ii) Plot 6, where the thickness of peat deposits on the coastal terrace is about 130–135 cm. In Plot 1 and 2 (forest-tundra), the maximum thawing depth of peat mounds, at the time of sampling, was 50–55 cm. On other plots—3 and 4 (southern tundra), 5 and 6 (northern tundra)—peat deposits thawed to a depth of 26–32 cm. The absence of clearly defined trends in the changes in the thawing depths of peat layers along the sequence of peat plateaus from the Barents Sea Coast to the southern tundra is probably specified by different weather conditions in years of observation. Peat samples from the plots were collected across years with different weather conditions (Table 2).
2.2. Sample Collection and Laboratory Studies
Field and laboratory studies were carried out according to the classical methods of soil science and soil microbiology. In each case, sampling was conducted either in the last decade of July or in the first decade of August. Peat samples from the active layers were collected layer by layer according to the botanical composition and the degree of decomposition of peat. Samples from permafrost layers were collected by hand drilling every 10 cm to a depth of 1 m, every time going below 20 cm. During the sampling, conditions were observed to prevent biological contamination of samples. Before the beginning of microbiological studies, peat samples were preserved by deep freeze (−18 to −20 °C). In total, 94 samples were analyzed.
To characterize the culturable part of microfungi, the method of serial dilutions of a soil suspension was used taking into account the number of microorganisms giving rise to colonies on various diagnostic media [58]. Isolation and registration of microfungi was performed on acidified Czapek’s medium (pH = 4.5), Hutchinson’s medium, Sabouraud’s medium and wort agar at different temperatures of thawing of frozen peat samples (+25, +35, +52 °C) and cultivation of seeding (+4, +25 °C) [25,31]. Soil suspensions were prepared with three serial 3-fold dilutions with 3-fold seeding on Petri dishes from each dilution. Therefore, it was 21-fold seeding of the soil suspension on a solid nutrient medium for each temperature of defrosting and cultivation. Taxonomic identification, using morphology of fungal isolates, was performed according to [59,60,61,62,63,64]. The names and positions of taxa were unified using MycoBank [65] and Index Fungorum [66] databases.
2.3. Statistical Analysis
To characterize the mycobiota, statistical analysis was performed by calculating the Shannon-Weaver species diversity index (Shannon-Weaver: H1 = −∑pilogpi), Pielou’s evenness index (Pielou: E = H1/lnN), Simpson’s dominance index (Simpson: D = 1 − (∑ni(ni − 1)/N(N − 1)) and the polydominance index (S) [67], as well as indicators of species frequency and abundance [68]. The similarities among fungal taxa from different plots were estimated using the Sorensen-Chekanovsky coefficient (Cs). Statistical processing of obtained results was carried out using the ExcelToR plugin for Microsoft Excel [69]. Cluster analysis was used for statistical processing of the array of data on the species diversity of culturable microscopic fungi isolated from various layers of peat deposits. Hierarchical cluster analysis allows us to identify groups (clusters) of objects similar to each other, and to identify hierarchical relationships between the selected groups. As a similar measure, we used the Manhattan (block) distance to calculate the modulus of the difference between all the characteristics of the objects (points) under study, and as a grouping method, we used the Ward method, which minimizes intragroup variance.
3. Results and Discussions
3.1. Taxonomic Diversity
In total, the complex of culturable microfungi inhabiting peatlands of the European Northeast of Russia is characterized by high taxonomic diversity (H = 2.78), high values of evenness (E = 0.63) and high values of the Simpson index (S = 0.90). During the study, eighty-three fungal species from seventeen genera and two forms of Mycelia sterilia were isolated from peat samples (Figure 3, Table 3). In the phylum Mucoromycota, fifteen species (18% of total isolate number) were retrieved, and these species were distributed by genus: Mucor (four), Mortierella (seven), Umbelopsis (three), Podila (one). The phylum Ascomycota is most represented (sixty-eight species from thirteen genera). The genus Penicillium dominates the species saturation (thirty-seven species, 44% of total isolate number), followed by the genera Aspergillus (five species), Talaromyces (five), Oidiodendron (five), Trichoderma (four), Chaetomium (three), Cladosporium (two), single Aureobasidium (one), Chrysosporium (one), Cephalosporium (one), Pseudogymnoascus (one) (Table 3). Unidentified isolates of Mycelia sterilia are observed as part of groups of pigmented and albino (non-pigmented) Mycelia sterilia [70]. Currently, researchers are actively using molecular genetic methods [2,47]. These methods allow us to identify fungal species whose colonies do not form sporulation on the media used. In our further studies, we plan to use molecular genetic methods to clarify the species composition of fungal communities in tundra and forest-tundra peatlands.
The structure of microfungal complex in permafrost peatlands is represented by rare species (51%), random species (32%), frequent species (15%) and dominant species (2%). Peatlands are dominated by Penicillium canescens (72%) and albino Mycelia sterilia (61%). The high percentage of dominance of Mycelia sterilia is a response to cold stress, which stimulates the synthesis of melanin-like pigments, with the formation of highly melanized or sterile hyphae [19].
According to relative abundance, permafrost peatlands are dominated by Talaromyces funiculosus (41%), Pseudogymnoascus pannorum (36%), albino Mycelia sterilia (29%), Umbelopsis vinacea (25%), Mortierella alpina (17%), Penicillium decumbens (21%), P. spinulosum (20%), P. canescens (17%). All these species are typical species of soil fungal communities in Arctic and Subarctic terrestrial ecosystems [4,5,54,71,72,73].
In the direction from south to north, not only the total number of identified species of fungi decreases, but also the species saturation of their leading genus (Figure 4). The genus Penicillium (thirty-five species) is most saturated with species in the peatlands of the forest tundra. In the peatlands of the northern tundra, the species saturation of the genus Penicillium is reduced to thirteen species of fungi.
3.2. Diversity of Fungi in Active and Permafrost Layers
The species diversity of microfungi in the active layers of the studied peatlands is represented by seventy-three species (H = 2.96, E = 0.69, S = 0.95). The phylum Ascomycota includes 87% of the total number of species. For Ascomycota, the genus Penicillium is distinguished by the largest number of species (twenty-nine species, or 40% of the total number of species). Dominance in the number of species belonging to the genus Penicillium is typical for the peat soils of the plain and mountain landscapes of the Arctic and Subarctic [4,54,74,75].
The phylum Mucoromycota includes fourteen species (19% of the total number of identified species) with dominated species belonging to the genus Mortierella (seven species). The main concentration of species belonging to Mucoromycota in the active layers is caused by their capability to decompose cellulose and polyphenolic compounds. The abundance of species from Mucoromycota in peatlands is due to these species having resistant and thick-walled spores, which allow them to survive for a long time [76].
Dominance of species belonging to the genus Mortierella among Mucoromycota is due to their capability to active chitin decomposition, a major component of fungal hyphae [77]. Diversity of invasive species belonging to the genus Aspergillus is mainly detected in the active layers of permafrost-affected peatlands. Moreover, Aspergillus (five species) is the most species-rich in forest-tundra peatlands [4]; no species of this genus were detected in the active layer of southern tundra peatlands [54]. Previous studies showed that the genus Aspergillus is represented by no more than one to four species in the plain tundra and mountain soils of the Arctic and Subarctic [54,74]. Aspergillus versicolor was not found in the studied plots. However, those species have been previously isolated from tundra soils of the Polar Urals and the European Northeast of Russia, according to [56,78]. Those species are mainly found in aquatic habitats [79,80]. In the active layers of peatland, in Plot 3, species from the genus Chaetomium (Chaetomium globosum) were identified [54]. These species are characterized by cellulase activity, high competitive ability and high growth rate dynamics. They are capable of producing toxic metabolites, according to data found in the literature and the results of studies of their morphological, cultural and biodestructive peculiarities [81].
As illustrated in Figure 5, the largest species diversity of microfungi was detected in the upper (active) layers of peatlands [4,5,54]. The horizontal differentiation of fungi within peatlands is basically due to changes in vegetation cover, peat chemical composition, and structure of permafrost layers [82]. The active layers of peatlands on the European Northeast of Russia are dominated by the following species: albino Mycelia sterilia (81%), Pseudogymnoascus pannorum (68%), Penicillium simplicissimum (65%), Penicillium sp. (65%), Umbelopsis vinacea (65%). The ratio of dominants varies according to the location of the plots. In forest-tundra (Plots 1 and 2), the active layers of peatlands are dominated by Pseudogymnoascus pannorum (82%), albino Mycelia sterilia (82%), Mortierella alpina (64%), Mortierella sp. (64%), Umbelopsis vinacea (64%). In southern tundra (Plot 3 and 4), the active layers of peatlands are dominated by Talaromyces funiculosus (38%) and albino Mycelia sterilia (33%). In northern tundra (Plots 5 and 6), the dominants are albino Mycelia sterilia (89%), Penicillium simplicissimum (78%), Penicillium decumbens (78%), Umbelopsis vinacea (67%). Most species of microfungi were isolated from the active layers of peatlands in forest-tundra (sixty-four species, H = 2.84), as shown in Table 4. In the southern and northern tundra peatlands, fungal species diversity is decreased by 2.7–3.0 times (H = 2.53). The smallest number of fungal species is isolated from the active layers of peatlands in northern tundra (twenty species, H = 2.38). Fungal communities of peatlands in southern and northern tundra are characterized by the maximum values of evenness index of the fungal community (E = 0.79–0.80).
According to relative species abundance, the active layers of peatlands are slightly different. In forest-tundra, abundant species are Penicillium thomii (14%), albino Mycelia sterilia (13%), Penicillium spinulosum (13%), P. simplicissimum (13%); in southern tundra, Talaromyces funiculosus (21%), albino Mycelia sterilia (15%), Umbelopsis vinacea (14%); in northern tundra, Penicillium decumbens (23%), P. canescens (17%), P. thomii (13%). In the active layers of peatlands of the European Northeast of Russia, according to the frequency of species occurrence, the basis of microfungal communities are random species (64%), while the share of rare, frequent and dominant species accounts for 19%, 8% and 7%, respectively. This is typical for peatlands in forest-tundra and tundra [4,54].
The upper part of the active layer of peatlands (a depth of 0–10 cm) is characterized by the largest number of diverse fungal species. However, in the direction from south to north, the number of species decreases in this part of the active layer. The following number ranges of species have been identified in these different environs: forest-tundra (thirty-three to thirty-four species), southern tundra (eight to fourteen species), northern tundra (eleven to fourteen species). In peatlands, at the active layer/permafrost border (20 cm below), the number of isolated species sharply decreases to zero to five species.
Permafrost layers of peat deposits are characterized by lower fungal species diversity. Specifically, thirty-seven species were isolated from the permafrost layers of peatlands in forest-tundra, followed by southern tundra (twenty-four to twenty-six species), and northern tundra (four species only). The fungal community in permafrost layers of the northern tundra peatlands is characterized by the lowest values of the indices H, E, S (1-D), S1/D (0.67; 0.49; 0.01; 100) if compared to forest-tundra and southern tundra peatlands (Table 4).
In permafrost layers of forest-tundra peatlands, abundant species are Penicillium spinulosum (17%), Talaromyces funiculosus (34%), Umbelopsis vinacea (15%); in southern tundra, Pseudogymnoascus pannorum (30%), Mortierella alpina (28%); in northern tundra, Pseudogymnoascus pannorum (80%). The permafrost layers of southern tundra peatlands are characterized by the presence of microscopic fungi belonging to the genus Chaetomium—Chaetomium spirale, Chaetomium sp. Many fungal species from the genus Chaetomium actively destroy cellulose [83]. Fungal species isolated from the permafrost layers of northern tundra peatlands (Aureobasidium pullulans, Pseudogymnoascus pannorum, albino Mycelia sterilia, pigmented Mycelia sterilia) are typical for the permafrost-affected soils of the European Northeast of Russia [4,5,54]. Members of the species Aureobasidium pullulans are known as rocky-substrate dwellers and they dominate the soils of sparse plant communities of the Arctic and Antarctic [70,74]. They are known for actively developing at low temperatures with weak production of organic acids (oxalic acid, fumaric acid, malic acid, succinic acid, glyceric acid) [7]. It is known that some organic acids produced by fungi, under conditions of nutrient deficiency, can be absorbed by the mycelium and used as a carbon source for the biosynthesis of other products. Succinic, malic and citric acids are easily consumed as the only carbon source by fungi from the genera Alternaria, Botrytis, Cladosporium and Penicillium [84]. The species Pseudogymnoascus pannorum exhibit psychrotolerant and halotolerant properties at low temperatures, as evidenced by their presence in cryopags, marine sediments and soils of coastal areas of Antarctica [30,85]. The tolerance of Pseudogymnoascus pannorum for the extreme conditions of low temperatures is associated with their ability to produce a large amount of polyunsaturated fatty acids under stress [34].
Culturable fungi associated with mineral layers (G horizons) underlying peat deposits within peat plateaus were identified only for Plot 1 (forest-tundra). Three fungi species were here isolated and identified from samples of mineral layers (a depth of 238–258 cm): Mucor hiemalis, Mucor racemosus and Mucor sp. Fungi associated with mineral layers of Plot 3, 4 (southern tundra) and Plot 5, 6 (northern tundra) did not give rise to colonies under the cultivation conditions.
3.3. Statistical Analysis
In total, the complexes of culturable microfungi in the peatlands of the European Northeast of Russia have a certain species composition depending on the location of the peatland in some bioclimatic zone/subzone. The Sorensen-Chekanovsky coefficient (Cs) varies from 45% to 56% between different couples of soils. For the fungal communities of peatlands in forest-tundra and southern tundra, Cs is 56%; in the southern and northern tundra, Cs is 52%.
Cluster analysis showed that the communities of culturable fungi in the studied peatlands form two clusters according to the composition of fungal species (Figure 6). The first cluster is formed by complexes of culturable fungi isolated from peatlands of Plot 1 and active layer of Plot 2, which is close in peat botanical composition to the active layer of Plot 1. The second cluster is formed by fungal communities from all other plots. Moreover, the fungal complexes from the active layers of peatlands in southern (Plots 3 and 4) and northern (Plots 5 and 6) tundra form one group, and the fungal complexes from the permafrost layers, including the mineral layer of Plot 1 and permafrost layer of Plot 2, are combined into another group. This indicates the specific formation of culturable fungal complexes in the active layers of peatlands in forest tundra, as well as active and permafrost layers of peatlands in tundra.
4. Conclusions
In this study, the diversity of microscopic fungi complexes in the permafrost-affected peatlands of the European Northeast was assessed. We have compiled a list of culturable fungal species. Currently, it includes eighty-three species of fungi from seventeen genera and two forms of Mycelia sterilia (pigmented and albino mycelia). The basis of the complex is represented by anamorphic species belonging to the phylum Ascomycota (sixty-eight species) and Mucoromycota is represented by fifteen species. According to the number of species, all genera form the following sequence: Penicillium (thirty-seven species), Mortierella (seven), Talaromyces (six), Oidiodendron (five), Aspergillus (five), Mucor (four), Trichoderma (four), and other genera include one to three species. All microfungal complexes were characterized by a high abundance of species belonging to the genera Penicillium (Penicillium canescens 13–18%, P. simplicissimum 8–43%, P. spinulosum 6–17%), Pseudogymnoascus pannorum (13–31%) and Mycelia sterilia (18–35%). Differences in the diversity of fungi between active and permafrost layers of peat deposits were determined. It was shown that under cultivation conditions, colony growth of microscopic fungi did not occur in the mineral layers underlying the peat deposits of permafrost-affected peatlands in southern tundra and northern tundra. Our studies have revealed the clearly expressed tendency to decrease the species diversity of culturable microscopic fungi in permafrost peatlands in the direction from the forest-tundra to the northern tundra. Currently, hydrocarbon deposits are being actively developed in the Arctic and Subarctic of the European Northeast. This can lead to mechanical disturbance of peat plateaus in tundra and forest tundra, their contamination with oil waste and other pollutants, and the destruction of the composition, structure and diversity of soil microscopic fungi. Since, within this study, we investigated natural peatlands unaffected by technogenic impact, these findings on the composition of microscopic fungi can be the basis for environmental monitoring of frozen bogs on the European Northeast, disturbed by industrial development of the Arctic and Subarctic.
Conceptualization, E.M.L. and Y.A.V.; Methodology, Validation, V.A.K., Y.A.V. and E.M.P.; Software, Y.A.V. and O.V.S.; Formal Analysis, Y.A.V., V.A.K. and E.M.L.; Investigation, V.A.K.; Visualization, O.V.S., Y.A.V. and E.M.L.; Resources, E.M.L.; Data Curation, E.M.L.; Writing—Original Draft Preparation, Y.A.V., V.A.K. and O.V.S., Writing—Review and Editing, Y.A.V., O.V.S. and E.M.L.; Supervision, E.M.L.; Project Administration, E.M.L.; Funding Acquisition, E.M.L. All authors have read and agreed to the published version of the manuscript.
Not applicable.
The data presented in this study are available on request from the corresponding author.
The authors declare no conflict of interest.
Footnotes
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Enlarge this image.Figure 1. Location of the studied plots. The black frame shows the investigation area (a). The numbers indicate the plot IDs (b). Forest-tundra zone (Plot 1 and 2), southern shrub tundra subzone (Plot 3 and 4) and typical northern tundra subzone (Plot 5 and 6).
Enlarge this image.Figure 2. View of peat plateaus landscapes. Forest-tundra zone (Plot 1 and 2), southern shrub tundra subzone (Plot 3 and 4) and typical northern tundra subzone (Plot 5 and 6). All plots are described at Table 1.
Enlarge this image.Figure 3. Taxonomic diversity of culturable microscopic fungi in peatlands of the European Northeast. The numbers show the total number of species from genera belonging to the phyla Mucoromycota (a) and Ascomycota (b).
Enlarge this image.Figure 4. The change in the diversity and species saturation of genera of microscopic fungi along the sequence of peatlands of the European Northeast. Forest tundra (Plot 1 and 2)—southern tundra (Plot 3 and 4)—northern tundra (Plot 5 and 6). Abbreviations: FT – forest-tundra, ST – southern tundra, NT – northern tundra. All plots are described in Table 1. The numbers show the total number of species.
Enlarge this image.Figure 5. Changing the microfungal species diversity across the profile of peat deposits along the sequence of peatlands of the European Northeast. Forest tundra (Plot 1 and 2)—southern tundra (Plot 3 and 4)—northern tundra (Plot 5 and 6). Abbreviations: AL—active layer, PL—permafrost peat layer, ML—permafrost mineral layer. All plots are described at Table 1.
Enlarge this image.Figure 6. Dendrogram of similarity of microfungal complexes in the peatlands of the European Northeast (Ward clustering, Manhattan distance). Plots 1–6 (all plots are described at Table 1). Abbreviations: AL—active layer, PL—permafrost layer, ML—mineral layer.
Brief description of sampling plots.
| Plot ID | Sampling Year | Bioclimatic Zone/Subzone, Location | Coordinates | Peat Thickness, cm | Depth of Seasonal Thawing, cm |
|---|---|---|---|---|---|
| Plot 1 | 2016 | Forest-tundra, Nenets Autonomous Okrug (NAO), lower reaches of the Pechora river, riverine sloping hill of the watershed | 67°40′ N |
238 | 50 |
| Plot 2 | 2015 | Forest-tundra, NAO, lower reaches of the Pechora river, oldest alluvial terrace | 67°39′ N |
* | 55 |
| Plot 3 | 2019 | Southern tundra, The Komi Republic, Vorkuta district | 67°45′ N |
236 | 26 |
| Plot 4 | 2017 | Southern tundra-northern tundra ecotone belt, NAO, basin of the upper reaches of the Korotaikha river | 68°02′ N |
265 | 32 |
| Plot 5 | 2021 | Northern tundra, NAO, left bank of the lower reaches of the Korotaikha river, the Puntoty lake surroundings | 68°17′ N |
246 | 30 |
| Plot 6 | 2018 | Northern tundra, NAO, the Barents Sea Coast, marine terrace, polygonal tundra | 68°35′ N |
131 | 28 |
* Peat samples were collected from Plot 2 only to a depth of 115 cm.
Some weather parameters observed at Vorkuta weather station across years.
| Observaton Year | Temperature, °C | Total Precipitation, mm | ||||||
|---|---|---|---|---|---|---|---|---|
| I-XII 1 | VI-VII 2 | VII 3 | VIII 4 | I-XII 1 | VI-VII 2 | VII 3 | VIII 4 | |
| 2015 | −3.8 | 10.4 | 10.2 | 9.2 | 448 | 159.4 | 95.0 | 22.7 |
| 2016 | −1.1 | 14.4 | 18.8 | 12.9 | 441.5 | 160.3 | 13.5 | 99.0 |
| 2017 | −4.8 | 11.6 | 16.8 | 9.3 | 524.1 | 128.6 | 8.3 | 81.7 |
| 2018 | −3.9 | 10.7 | 15.2 | 9.7 | 747.3 | 146.0 | 19.1 | 85.6 |
| 2019 | −3.7 | 10.0 | 15.3 | 9.9 | 667.2 | 176.1 | 63.9 | 58.4 |
| 2020 | −1.6 | 11.8 | 15.0 | 12.2 | 670.4 | 120.2 | 37.4 | 13.2 |
| 2021 | −2.4 | 11.0 | 11.5 | 12.5 | 506.4 | 138.2 | 53.7 | 26.2 |
| 1990–2020 5 | −4.7 | 10.2 | 13.5 | 9.9 | 547 | 167.6 | 52.5 | 63.4 |
1 average annual temperature and total precipitation (January–December); 2 average temperature summer temperature and total precipitation (June–August); 3 average temperature and total precipitation for July; 4 average temperature and total precipitation for August; 5 multi-year (30 years) average parameters 1990–2020.
List of culturable fungi associated with peatlands from different bioclimatic zones/subzones of the European Northeast of Russia.
| Bioclimatic Zone/Subzone | ||
|---|---|---|
| Forest-Tundra | Southern Tundra | Northern Tundra |
| Penicillium aurantiogriseum Dierckx, P. canescens Sopp, P. citreonigrum Dierckx, P. granulatum Bainier, P. lanosum Westling, P. simplicissimum Thom, P. spinulosum Thom, P. thomii K.M. Zaleski, Penicillium sp., Pseudogymnoascus pannorum (Link) Minnis & D.L. Lindne, Umbelopsis vinacea Arx, Mortierella sp., Mucor hiemalis Wehmer, Mucor sp., Talaromyces funiculosus (Thom) Samson, N. Yilmaz, Frisvad & Seifert, N. Yilmaz, Frisvad & Seifert, albino Mycelia sterilia, pigmented Mycelia sterilia | ||
| Aspergillus flavus Link, Aspergillus fumigatus Fresen., Chrysosporium merdarium (Ehrenb.) J.W. Carmich., Cladosporium cladosporioides (Fresen.) G.A. de Vries, Cl. herbarum (Pers.) Link, Mortierella alpina Peyron, M. polycephala Coem., Mucor racemosus Bull., Mucor sp. Penicillium dierckxii Biourge, P. implicatum Biourge, P. lividum Westling, P. olivicolor Pitt, P. waksmanii K.W. Zaleski, Talaromyces diversus (Raper & Fennell) Samson, N. Yilmaz & Frisvad, T. rugulosus (Thom) Samson, Trichoderma viride Schumach. | Aureobasidium pullulans (de Bary & Löwenthal) G. ArnaudG. Arnaud, Talaromyces stipitatus C.R. Benj. | |
| Alternaria tenuis Nees, Aspergillus niger Tiegh., A. ochraceus G. Wilh., Aspergillus sp., Cephalosporium terricola Kamyschko, Mortierella horticola Linnem., M. biramosa Tiegh., M. pygmaea Chalab., M. verticillata Linnem., Oidiodendron tenuissimum (Peck) S. Hughes, O. gracile Zhdanova, O. griseum Robak, Oidiodendron sp., Penicillium citrinum Thom, P. commune Thom, P. digitatum Sacc., P. frequentans Westling, P. glaucum Link, P. hirsutum Dierckx, P. italicum Wehmer, P. jensenii K.W. Zaleski, P. lapidosum Raper & Fennell, P. miczynskii K.W. Zaleski, P. oxalicum Currie & Thom, P. phoeniceum J.F.H. Beyma, P. raistrickii G. Sm., P. restrictum J.C. Gilman & E.V. Abbott, P. turbatum Westling 1911, P. roqueforti Thom, P. velutinum Terui & Shibas., P. verrucosum Dierckx, P. vinaceum J.C. Gilman & E.V. Abbott, Podila minutissima (Tiegh.) Vandepol & Bonito Talaromyces variabilis (Sopp) Samson, N. Yilmaz, Frisvad & Seifert, T. verruculosus (Peyronel) Samson, N. Yilmaz, Frisvad & Seifert, Tolypocladium inflatum W. Gams, Trichoderma aureoviride Rifai, Trichoderma sp., Umbelopsis isabellina W.Gams, U. ramanniana W.Gams | Mucor circinelloides Tiegh., Chaetomium globosum Kunze, Ch. spirale Zopf, Chaetomium sp., Oidiodendron majus G.L. Barron, Penicillium glabrum (Wehmer) Westling, Trichoderma koningii Oudemans | |
| Penicillium camemberti Sopp, P. decumbens Thom, |
Penicillium camemberti Sopp, P. decumbens Thom, |
|
Indicators of the structure of microfungal complex in active and permafrost layers of peat deposits along the sequence of peatlands. Forest tundra (Plots 1 and 2) → southern tundra (Plots 3 and 4) → northern tundra (Plots 5 and 6).
| Indices | Plots | ||||||||
|---|---|---|---|---|---|---|---|---|---|
| 1, 2 | 3, 4 | 5, 6 | 1, 2 | 3, 4 | 5, 6 | 1, 2 | 3, 4 | 5, 6 | |
| Active Layer | Permafrost Layer | Mineral Layer | |||||||
| The total number of isolated species | 64 | 24 | 20 | 37 | 26 | 4 | 3 | 0 | 0 |
| Shannon species diversity index (H) | 2.84 | 2.53 | 2.38 | 2.09 | 2.06 | 0.67 | 0.43 | 0 | 0 |
| Pielou’s evenness index (E) | 0.68 | 0.80 | 0.79 | 0.58 | 0.63 | 0.49 | 0.39 | 0 | 0 |
| Simpson’s dominance index (S) (1-D) | 0.91 | 0.89 | 0.88 | 0.84 | 0.83 | 0.01 | 0.97 | 0 | 0 |
| Williams polydominance index (1/D) | 11.27 | 9.44 | 8.18 | 6.07 | 5.97 | 100.00 | 30.46 | 0 | 0 |
References
1. Ji, X.; Abakumov, E.; Chigray, S.; Saparova, S.; Polyakov, V.; Wang, W.; Wu, D.; Li, C.; Huang, Y.; Xie, X. Response of carbon and microbial properties to risk elements pollution in arctic soils. J. Hazard. Mater.; 2020; 408, 124430. [DOI: https://dx.doi.org/10.1016/j.jhazmat.2020.124430] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/33176958]
2. Xue, D.; Liu, T.; Chen, H.; Liu, J.; Hu, J.; Liu, L. Fungi are more sensitive than bacteria to drainage in the peatlands of the Zoige Plateau. Ecol. Indic.; 2021; 124, 107367. [DOI: https://dx.doi.org/10.1016/j.ecolind.2021.107367]
3. Lapteva, E.M.; Kovaleva, V.A.; Vinogradova, Y.A.; Kaverin, D.A.; Pastukhov, A.V. Micromycetes in peat soils of palsa mires in the forest-tundra zone. Vestn. Inst. Biol.; 2017; 3, pp. 30-36. (In Russian)
4. Vinogradova, Y.A.; Lapteva, E.M.; Kovaleva, V.A.; Perminova, E.M. Profile distribution pattern of microfungi in the per-mafrost-affected peatland of forest-tundra. Mikol. Fitopatol.; 2019; 53, pp. 342-353. (In Russian)
5. Vinogradova, Y.A.; Lapteva, E.M.; Kovaleva, V.A.; Perminova, E.M. Soil fungi biomass and diversity of soil microfungi in the active layer of south tundra peatlands. Mikol. Fitopatol.; 2021; 55, pp. 105-118. (In Russian)
6. Andersen, R.; Chapman, S.; Artz, R. Microbial communities in natural and disturbed peatlands: A review. Soil Biol. Biochem.; 2013; 57, pp. 979-994. [DOI: https://dx.doi.org/10.1016/j.soilbio.2012.10.003]
7. Sazanova, K.V. Organic Acids of Fungi and Their Ecological and Physiological Significance. Ph.D. Thesis; Saint Petersburg State University: Saint Petersburg, Russia, 2014; (In Russian)
8. Fenner, N.; Ostle, N.J.; McNamara, N.; Sparks, T.; Harmens, H.; Reynolds, B.; Freeman, C. Elevated CO2 Effects on Peatland Plant Community Carbon Dynamics and DOC Production. Ecosystems; 2007; 10, pp. 635-647. [DOI: https://dx.doi.org/10.1007/s10021-007-9051-x]
9. Kostadinova, N.; Tosi, S.; Spassova, B.; Angelova, M. Comparison of the oxidative stress response of two Antarctic fungi to different growth temperatures. Pol. Polar Res.; 2017; 38, pp. 393-408. [DOI: https://dx.doi.org/10.1515/popore-2017-0015]
10. Juan-Ovejero, R.; Briones, M.; Öpik, M. Fungal diversity in peatlands and its contribution to carbon cycling. Appl. Soil Ecol.; 2019; 146, 103393. [DOI: https://dx.doi.org/10.1016/j.apsoil.2019.103393]
11. Hogg, I.D.; Cary, C.S.; Convey, P.; Newsham, K.K.; O’Donnell, A.G.; Adams, B.J.; Aislabie, J.; Frati, F.; Stevens, M.I.; Wall, D.H. Biotic interactions in Antarctic terrestrial ecosystems: Are they a factor?. Soil Biol. Biochem.; 2006; 38, pp. 3035-3040. [DOI: https://dx.doi.org/10.1016/j.soilbio.2006.04.026]
12. Bell, T.H.; Callender, K.L.; Whyte, L.G.; Greer, C.W. Microbial Competition in Polar Soils: A Review of an Understudied but Potentially Important Control on Productivity. Biology; 2013; 2, pp. 533-554. [DOI: https://dx.doi.org/10.3390/biology2020533] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/24832797]
13. Kravchenko, I.; Grouzdev, D.; Sukhacheva, M.; Minayeva, T.; Sirin, A. Microbial Communities of Peaty Permafrost Tundra Soils along the Gradient of Environmental Conditions and Anthropogenic Disturbance in Pechora River Delta in the Eastern European Arctic. Diversity; 2023; 15, 251. [DOI: https://dx.doi.org/10.3390/d15020251]
14. Tosi, S.; Onofri, S.; Brusoni, M.; Zucconi, L.; Vishniac, H. Response of the Antarctic soil fungal assemblages to the experi-mental warming and reduction of UV radiation. Polar Biol.; 2005; 28, pp. 470-482. [DOI: https://dx.doi.org/10.1007/s00300-004-0698-x]
15. Eichholz, I.; Huyskens-Keil, S.; Keller, A.; Ulrich, D.; Kroh, L.W.; Rohn, S. UV-B-induced changes of volatile metabolites and phenolic compounds in blueberries (Vaccinium corymbosum L.). Food Chem.; 2011; 126, pp. 60-64. [DOI: https://dx.doi.org/10.1016/j.foodchem.2010.10.071]
16. Villarreal, P.; Carrasco, M.; Barahona, S.; Alcaino, J.; Cifuentes, V.; Baeza, M. Tolerance to ultraviolet radiation of psychrot-olerant yeasts and analysis of their carotenoid, mycosporine, and ergosterol content. Curr. Microbiol.; 2016; 72, pp. 94-101. [DOI: https://dx.doi.org/10.1007/s00284-015-0928-1] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/26483082]
17. Callaghan, T.V.; Jonasson, S.; Nichols, H.; Heywood, R.B.; Wookey, P.A. The Arctic and environmental change. Philos. Trans. Royal Soc. A; 1995; 352, pp. 259-276.
18. Zucconi, L.; Pagano, S.; Fenice, M.; Selbmann, L.; Tosi, S.; Onofri, S. Growth temperature preferences of fungal strains from Victoria Land, Antarctica. Polar Biol.; 1996; 16, pp. 53-61. [DOI: https://dx.doi.org/10.1007/BF02388735]
19. Ruisi, S.; Barreca, D.; Selbmann, L.; Zucconi, L.; Onofri, S. Fungi in Antarctica. Rev. Environ. Sci. Biotechnol.; 2007; 6, pp. 127-141. [DOI: https://dx.doi.org/10.1007/s11157-006-9107-y]
20. Arenz, B.E.; Blachette, R.A. Distribution and abundance of soil fungi in Antarctica at sites of the Peninsula, Ross Sea region and McMudo Dry Valleys. Soil Biol. Biochem.; 2011; 43, pp. 308-315. [DOI: https://dx.doi.org/10.1016/j.soilbio.2010.10.016]
21. Gittel, A.; Bárta, J.; Kohoutová, I.; Schnecker, J.; Wild, B.; Capek, P.; Kaiser, C.H.; Torsvik, V.; Richter, A.; Schleper, C.H. et al. Site-and horizon-specific patterns of microbial community structure and enzyme activities in permafrost-affected soils of Greenland. Front. Microbiol.; 2014; 5, 541. [DOI: https://dx.doi.org/10.3389/fmicb.2014.00541]
22. Deng, J.; Gu, Y.; Zhang, J.; Xue, K.; Qin, Y.; Yuan, M.; Yin, H.; He, Z.; Schuur, E.A.G.; Tiedje, J.M. et al. Shifts of tundra bacterial and archael communities along a permafrost thaw gradient in Alaska. Mol. Ecol.; 2015; 24, pp. 222-234. [DOI: https://dx.doi.org/10.1111/mec.13015] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/25424441]
23. Yogabaanu, U.; Weber, J.F.; Convey, P.; Rizman-Idid, M.; Alias, S.A. Antimicrobial properties and the influence of tem-perature on secondary metabolite production in cold environment soil fungi. Polar Sci.; 2017; 14, pp. 60-67. [DOI: https://dx.doi.org/10.1016/j.polar.2017.09.005]
24. Müller, O.; Bang-Andreasen, T.; Iii, R.A.W.; Elberling, B.; Taş, N.; Kneafsey, T.; Jansson, J.K.; Øvreås, L. Disentangling the complexity of permafrost soil by using high resolution profiling of microbial community composition, key functions and respiration rates. Environ. Microbiol.; 2018; 20, pp. 4328-4342. [DOI: https://dx.doi.org/10.1111/1462-2920.14348] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/29971895]
25. Ozerskaya, S.M.; Kochkina, G.A.; Ivanushkina, N.E.; Knyazeva, E.V.; Gilichinskii, D.A. The structure of micromycete com-plexes in permafrost and cryopegs of the arctic. Microbiologiya; 2008; 77, pp. 542-550. (In Russian)
26. Ozerskaya, S.M.; Kochkina, G.A.; Ivanushkina, N.E.; Gilichinsky, D.A. Fungi in Permafrost. Permafrost Soils; Margesin, R. Springer: Berlin/Heidelberg, Germany, 2009; pp. 85-95.
27. Zelenskaya, M.S.; Kirtsideli, I.Y.; Vlasov, D.Y.; Krylenkov, V.A.; Sokolov, V.T. Micromycetes—Biodestructors in Arctic bio-geocenoses. Probl. Reg. Ecol.; 2013; 5, pp. 135-140. (In Russian)
28. Onofri, S.; Selbmann, L.; Zucconi, L.; Pagano, S. Antarctic microfungi as models for exobiology. Planet. Space Sci.; 2004; 52, pp. 229-237. [DOI: https://dx.doi.org/10.1016/j.pss.2003.08.019]
29. Zucconi, L.; Selbmann, L.; Buzzini, P.; Turchetti, B.; Guglielmin, M.; Frisvad, J.C.; Onofri, S. Searching for eukaryotic life preserved in Antarctic permafrost. Polar Biol.; 2011; 35, pp. 749-757. [DOI: https://dx.doi.org/10.1007/s00300-011-1119-6]
30. Godinho, V.M.; Gonçalves, V.N.; Santiago, I.F.; Figueredo, H.M.; Vitoreli, G.A.; Schaefer, C.E.G.R.; Barbosa, E.C.; Oliveira, J.G.; Alves, T.M.A.; Zani, C. et al. Diversity and bioprospection of fungal community present in oligotrophic soil of continental Antarctica. Extremophiles; 2015; 19, pp. 585-596. [DOI: https://dx.doi.org/10.1007/s00792-015-0741-6]
31. Kochkina, G.A.; Ozerskaya, S.M.; Ivanushkina, N.E.; Chigineva, N.I.; Vasilenko, O.V.; Spirina, E.V.; Gilichinskii, D.A. Fungal diversity in the Antarctic active layer. Microbiology; 2014; 83, pp. 94-101. [DOI: https://dx.doi.org/10.1134/S002626171402012X]
32. Robinson, C.H.; Saunders, P.W.; Madan, N.J.; Pryce-Miller, E.J.; Pentecost, A. Does nitrogen deposition affect soil micro-fungal diversity and soil N and P dynamics in a high Arctic ecosystem?. Glob. Chang. Biol.; 2004; 10, pp. 1065-1079. [DOI: https://dx.doi.org/10.1111/j.1529-8817.2003.00793.x]
33. Blaud, A.; Lerch, T.Z.; Phoenix, G.K.; Osborn, A.M. Arctic soil microbial diversity in a changing world. Res. Microbiol.; 2015; 166, pp. 796-813. [DOI: https://dx.doi.org/10.1016/j.resmic.2015.07.013] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/26275598]
34. Weinstein, R.N.; Montiel, P.O.; Johnstone, K. Influence of growth temperature on lipid and soluble carbohydrate synthesis by fungi isolated from fellfield soil in the maritime Antarctic. Mycologia; 2000; 92, pp. 222-229. [DOI: https://dx.doi.org/10.1080/00275514.2000.12061148]
35. Onofri, S.; Fenice, M.; Cicalini, A.R.; Tosi, S.; Magrino, A.; Pagano, S.; Selbmann, L.; Zucconi, L.; Vishniac, H.S.; Ocampo-Friedmann, R. et al. Ecology and biology of microfungi from Antarctic rocks and soils. Ital. J. Zool.; 2000; 67, pp. 163-167. [DOI: https://dx.doi.org/10.1080/11250000009356372]
36. Tosi, S.; Casado, B.; Gerdol, R.; Caretta, G. Fungi isolated from Antarctic mosses. Polar Biol.; 2002; 25, pp. 262-268. [DOI: https://dx.doi.org/10.1007/s00300-001-0337-8]
37. Zucconi, L.; Ripa, C.; Selbmann, L.; Onofri, S. Effects of UV on the spores of the fungal species Arthrobotrys oligospora and A. ferox. Polar Biol.; 2002; 25, pp. 500-505.
38. Selbmann, L.; Isola, D.; Fenice, M.; Zucconi, L.; Sterflinger, K.; Onofri, S. Potential extinction of Antarctic endemic fungal species as a consequence of global warming. Sci. Total Environ.; 2012; 438, pp. 127-134. [DOI: https://dx.doi.org/10.1016/j.scitotenv.2012.08.027]
39. Selbmann, L.; Grube, M.; Onofri, S.; Isola, D.; Zucconi, L. Antarctic Epilithic Lichens as Niches for Black Meristematic Fungi. Biology; 2013; 2, pp. 784-797. [DOI: https://dx.doi.org/10.3390/biology2020784]
40. Vishniac, H.S.; Onofri, S. Cryptococcus antarcticus var. circumpolaris var. nov., a basidiomycetous yeast from Antarctica. Antonie Van. Leeuwenhoek; 2003; 83, pp. 231-233. [DOI: https://dx.doi.org/10.1023/a:1023369728237]
41. Tosi, S.; Kostadinova, N.; Krumova, E.; Pashova, S.; Dishliiska, V.; Spassova, B.; Vassilev, S.; Angelova, M. Antioxidant enzyme activity of filamentous fungi isolated from Livingston Island, Maritime Antarctica. Polar Biol.; 2010; 33, pp. 1227-1237. [DOI: https://dx.doi.org/10.1007/s00300-010-0812-1]
42. Krishnan, A.; Convey, P.; Gonzalez-Rocha, G.; Alias, S.A. Production of extracellular hydrolase enzymes by fungi from King George Island. Polar Biol.; 2014; 39, pp. 65-76. [DOI: https://dx.doi.org/10.1007/s00300-014-1606-7]
43. Song, Y.; Jiang, L.; Song, C.; Wang, X.; Ma, X.; Zhang, H.; Tan, W.; Gao, J.; Hou, A. Microbial abundance and enzymatic activity from tussock and shrub soil in permafrost peatland after 6-year warming. Ecol. Indic.; 2021; 126, 107589. [DOI: https://dx.doi.org/10.1016/j.ecolind.2021.107589]
44. Aksenov, A.S.; Shirokova, L.S.; Kisil, O.Y.; Kolesova, S.N.; Lim, A.G.; Kuzmina, D.; Pouillé, S.; Alexis, M.A.; Castrec-Rouelle, M.; Loiko, S.V. et al. Bacterial Number and Genetic Diversity in a Permafrost Peatland (Western Siberia): Testing a Link with Organic Matter Quality and Elementary Composition of a Peat Soil Profile. Diversity; 2021; 13, 328. [DOI: https://dx.doi.org/10.3390/d13070328]
45. Thormann, M.N. The Role of Fungi in Boreal Peatlands. Boreal Peatland Ecosystems; Wieder, R.K.; Vitt, D.H. Springer: Berlin/Heidelberg, Germany, 2006; pp. 101-123.
46. Asemaninejad, A.; Thorn, R.G.; Lindo, Z. Experimental Climate Change Modifies Degradative Succession in Boreal Peatland Fungal Communities. Microb. Ecol.; 2016; 73, pp. 521-531. [DOI: https://dx.doi.org/10.1007/s00248-016-0875-9]
47. Elliott, D.R.; Caporn, S.J.M.; Nwaishi, F.; Nilsson, H.; Sen, R. Bacterial and Fungal Communities in a Degraded Ombrotrophic Peatland Undergoing Natural and Managed Re-Vegetation. PLoS ONE; 2015; 10, e0124726. [DOI: https://dx.doi.org/10.1371/journal.pone.0124726] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/25969988]
48. Artz, R.; Anderson, I.; Chapman, S.; Hagn, A.; Schloter, M.; Potts, J.; Campbell, C. Changes in Fungal Community Compo-sition in Response to Vegetational Succession During the Natural Regeneration of Cutover Peatlands. Microb. Ecol.; 2007; 54, pp. 508-522. [DOI: https://dx.doi.org/10.1007/s00248-007-9220-7]
49. Dobrovolskaya, T.G.; Golovchenko, A.V.; Zvyagintsev, D.G.; Inisheva, L.I.; Kurakov, A.V.; Smagin, A.V.; Zenova, G.M.; Lysak, L.V.; Semenova, T.A.; Stepanov, A.L. et al. The Functioning of Complexes of Microorganisms in Raised Peat Bogs an Analysis of the Reasons for the Slow Decomposition of Peat; KMK Scientific Press Ltd.: Moscow, Russia, 2013; 128.(In Russian)
50. Golovchenko, A.V.; Semenova, T.A.; Anisimova, O.V.; Dobrovolskaya, T.G.; Glukhova, T.V.; Stepanov, A.L. The Structure of Microbial Communities in the Soils of Regressive Noncryosolic Bog. Eurasian Soil Sci.; 2020; 53, pp. 668-674. [DOI: https://dx.doi.org/10.1134/S1064229320050063]
51. Sizonenko, T.A.; Khabibullina, F.M.; Zagirova, S.V. Soil microbiota of meso-oligotrophic peatland of middle taiga. Mikol. Fitopatol.; 2016; 50, pp. 115-123. (In Russian)
52. Matyshak, G.V.; Bogatyrev, L.G.; Goncharova, O.Y.; Bobrik, A.A. Specific features of the development of soils of hydromorphic ecosystems in the northern taiga of Western Siberia under conditions of cryogenesis. Eurasian Soil Sci.; 2017; 50, pp. 1115-1124. [DOI: https://dx.doi.org/10.1134/S1064229317100064]
53. Yakushev, A.V.; Matyshak, G.V.; Tarkhov, M.O.; Kachalkin, A.V.; Sefilyan, A.R.; Petrov, D.G. Microbiological Characteristics of Bare Peat Circles on Flat-Topped Peat Mounds in the North of Western Siberia. Eurasian Soil Sci.; 2019; 52, pp. 1081-1090. [DOI: https://dx.doi.org/10.1134/S1064229319090114]
54. Vinogradova, Y.A.; Lapteva, E.M.; Kovaleva, V.A.; Perminova, E.M. Diversity of soil micromycetes in peat frozen soils of the southern tundra. Mikol. Fitopatol.; 2022; 56, pp. 155-169.
55. Kirtsideli, I.Y. Soil microfungi of the Barents Sea coast (near Varandey settlement). Nov. Sist. Nizshikh Rastenii; 2009; 43, pp. 113-121. [DOI: https://dx.doi.org/10.31111/nsnr/2009.43.113]
56. Kirtsideli, I.Y.; Vlasov, D.Y.; Barantsevich, E.P.; Krylenkov, V.A.; Sokolov, V.T. Microfungi from soil of polar island IzvestiaTsik (Kara sea). Mikol. Fitopatol.; 2014; 48, pp. 365-371. (In Russian)
57. Cui, H.-J.; Wang, G.-X.; Yang, Y.; Chang, R.-Y.; Ran, F. Soil microbial community composition and its driving factors in alpine grasslands along a mountain elevational gradient. J. Mt. Sci.; 2016; 13, pp. 1013-1023. [DOI: https://dx.doi.org/10.1007/s11629-015-3614-7]
58. Zvyagintsev, D.G. Methods of Soil Microbiology and Biochemistry; MGU: Moscow, Russia, 1991; 304.(In Russian)
59. Ellis, M.B. Dematiaceous Hyphomycetes; Kew, Commonwealth Mycological Institute: Surrey, UK, 1971.
60. Ramirez, C. Manual and Atlas of the Penicillia; Elsevier Biomedical Press: Amsterdam, The Netherlands, 1982; 874.
61. Egorova, L.N. Pochvennye Griby Dal’nego Vostoka: Gifomitsety (Soil Fungi of the Russian Far East: Hyphomycetes); Nauka: Leningrad, Russia, 1986; (In Russian)
62. Pitt, J. A Laboratory Guide to Common Penicillium Species; Commonwealth Scientific and Industrial Research Organization: North Wales, Australia, 1991.
63. Leksandrova, A.V.; Velikanov, L.L.; Sidorova, I.I. The key to determining the species of the genus Trichoderma. Mikol. Fitopatol.; 2006; 40, pp. 457-468. (In Russian)
64. Domsch, K.H.; Gams, W.; Anderson, T.-H. Compendium of Soil Fungi; IHW-Verlag: Eching, Germany, 2007.
65. Mycobank. The MycoBank Engine and Related Databases. 2021; Available online: http://www.mycobank.org (accessed on 18 August 2021).
66. Index Fungorum. Available online: https://www.indexfungorum.org/ (accessed on 20 March 2022).
67. Magurran, E. Ecological Diversity and Its Measurement; Princeton University Press: Princeton, NJ, USA, 1988.
68. Kurakov, A.V. Methods for Isolation and Characterization of Complexes of Microscopic Fungi in Terrestrial Ecosystems; Maks Press: Moscow, Russia, 2001; 92.(In Russian)
69. Novakovskij, A.V. The interaction between Excel and the statistical package R for data processing in ecology. Vestn. Inst. Biol.; 2016; 3, pp. 26-33. (In Russian)
70. Vlasov, D.Y.; Zelenskaya, M.S.; Kirtsideli, I.Y.; Abakumov, E.V.; Krylenkov, V.A.; Lukin, V.V. Fungi on the natural and anthropogenic substrates in West Antarctica. Mikol. Fitopatol.; 2012; 46, pp. 20-26. (In Russian)
71. Kochkina, G.A.; Ivanushkina, N.E.; Ozerskaya, S.M. Structure of mycobiota of permafrost. Mikol. Segodnya; 2011; 2, pp. 178-184. (In Russian)
72. Edgington, S.; Thompson, E.; Moore, D.; Hughes, K.A.; Bridge, P. Investigating the insecticidal potential of Geomyces (Myxotrichaceae: Helotiales) and Mortierella (Mortierellacea: Mortierellales) isolated from Antarctica. Springerplus; 2014; 3, 289. [DOI: https://dx.doi.org/10.1186/2193-1801-3-289]
73. Kirtsideli, I.Y. Microscopic fungi in the soils of Hays Island (Franz Josef Land). Nov. Sist. Nizs. Rast.; 2015; 49, pp. 151-160. (In Russian)
74. Kirtsideli, I.Y.; Abakumov, E.V.; Teshebaev, S.B.; Zelenskaya, M.S.; Vlasov, D.Y.; Krylenkov, V.A.; Ryabusheva, Y.V.; Sokolov, V.T.; Barantsevich, E.P. Microbial communities in areas of Arctic settlements. Hyg. Sanit.; 2016; 95, pp. 923-929. (In Russian) [DOI: https://dx.doi.org/10.18821/0016-9900-2016-95-10-923-929]
75. Lamit, L.J.; Romanowicz, K.; Potvin, L.R.; Rivers, A.; Singh, K.; Lennon, J.T.; Tringe, S.G.; Kane, E.S.; Lilleskov, E.A. Patterns and drivers of fungal community depth stratification in Sphagnum peat. FEMS Microbiol. Ecol.; 2017; 93, fix082. [DOI: https://dx.doi.org/10.1093/femsec/fix082] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/28854677]
76. Lin, X.; Green, S.; Tfaily, M.; Prakash, O.; Konstantinidis, K.T.; Corbett, J.E.; Chanton, J.P.; Cooper, W.T.; Kostka, J.E. Microbial Community Structure and Activity Linked to Contrasting Biogeochemical Gradients in Bog and Fen Environments of the Glacial Lake Agassiz Peatland. Appl. Environ. Microbiol.; 2012; 78, pp. 7023-7031. [DOI: https://dx.doi.org/10.1128/AEM.01750-12] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/22843538]
77. Kim, Y.-J.; Zhao, Y.; Oh, K.-T.; Nguyen, V.-N.; Park, R.-D. Enzymatic deacetylation of chitin by extracellular chitin deacetylase from a newly screened Mortierella sp. DY-52. J. Microbiol. Biotechnol.; 2008; 18, pp. 759-766.
78. Khabibullina, F.M. Soil Mycobiota of Natural and Anthropogenic Disturbed Ecosystems of the North-East of the European Part of Russia. Doctor’s Thesis; IB FRC Komi SC UB RAS: Syktyvkar, Russia, 2009; (In Russian)
79. Wu, Z.-H.; Liu, D.; Xu, Y.; Chen, J.-L.; Lin, W.-H. Antioxidant xanthones and anthraquinones isolated from a marine-derived fungus Aspergillus versicolor. Chin. J. Nat. Med.; 2018; 16, pp. 219-224. [DOI: https://dx.doi.org/10.1016/S1875-5364(18)30050-5]
80. Mohamed, G.A.; Ibrahim, S.R.; Asfour, H.Z. Antimicrobial metabolites from the endophytic fungus Aspergillus versicolor. Phytochem. Lett.; 2019; 35, pp. 152-155. [DOI: https://dx.doi.org/10.1016/j.phytol.2019.12.003]
81. Linnik, M.A. Species Diversity and Characteristics of Fungi of the Genus Chaetomium. Ph.D. Thesis; Lomonosov MSU: Moscow, Russian, 2012; (In Russian)
82. Lin, X.; Tfaily, M.M.; Steinweg, J.M.; Chanton, P.; Esson, K.; Yang, Z.K.; Chanton, J.P.; Cooper, W.; Schadt, C.W.; Kostka, J.E. Microbial Community Stratification Linked to Utilization of Carbohydrates and Phosphorus Limitation in a Boreal Peatland at Marcell Experimental Forest, Minnesota, USA. Appl. Environ. Microbiol.; 2014; 80, pp. 3518-3530. [DOI: https://dx.doi.org/10.1128/AEM.00205-14]
83. Vedenyapina, E.G.; Lebedeva, E.V.; Zachinyaeva, A.V.; Vorobyev, N.I. Micromycetes in waste recycling II. Mycological characteristics of compost obtained as a result of bioconversion of urban waste. Mikol. Fitopatol.; 2010; 44, pp. 205-216. (In Russian)
84. Shlychkova, D.M. Mechanism of Bio-Damage of Building Materials by Micromycetes in Historical and Cultural Monuments. Master’s Thesis; St. Petersburg State Polytechnic University. Institute of Civil Engineering: Saint Petersburg, Russia, 2014; (In Russian)
85. Osono, T.; Ueno, T.; Uchida, M.; Kanda, H. Abundance and diversity of fungi in relation to chemical changes in arctic moss profiles. Polar Sci.; 2011; 6, pp. 121-131. [DOI: https://dx.doi.org/10.1016/j.polar.2011.12.001]
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; Perminova, Evgenia M
; Shakhtarova, Olga V
; Lapteva, Elena M